PATTERNS AND MECHANISMS OF SELECTION ON A FAMILY-DIAGNOSTIC TRAIT: EVIDENCE FROM EXPERIMENTAL MANIPULATION AND LIFETIME FITNESS SELECTION GRADIENTS
Jeffrey K. Conner
Kellogg Biological Station and Department of Plant Biology, Michigan State University, 3700 East Gull Lake Drive, Hickory Corners, Michigan 49060
E-mail: [email protected]
Search for more papers by this authorAmber M. Rice
Kellogg Biological Station and Department of Plant Biology, Michigan State University, 3700 East Gull Lake Drive, Hickory Corners, Michigan 49060
Search for more papers by this authorChristy Stewart
Kellogg Biological Station and Department of Plant Biology, Michigan State University, 3700 East Gull Lake Drive, Hickory Corners, Michigan 49060
Search for more papers by this authorMartin T. Morgan>3
School of Biological Sciences, Washington State University, Pullman, Washington 99164–4236
Search for more papers by this authorJeffrey K. Conner
Kellogg Biological Station and Department of Plant Biology, Michigan State University, 3700 East Gull Lake Drive, Hickory Corners, Michigan 49060
E-mail: [email protected]
Search for more papers by this authorAmber M. Rice
Kellogg Biological Station and Department of Plant Biology, Michigan State University, 3700 East Gull Lake Drive, Hickory Corners, Michigan 49060
Search for more papers by this authorChristy Stewart
Kellogg Biological Station and Department of Plant Biology, Michigan State University, 3700 East Gull Lake Drive, Hickory Corners, Michigan 49060
Search for more papers by this authorMartin T. Morgan>3
School of Biological Sciences, Washington State University, Pullman, Washington 99164–4236
Search for more papers by this authorAbstract
Abstract Plant traits that show little variation across higher taxa are often used as diagnostic traits, but the reason for the stasis of such traits remains unclear. Wild radish, Raphanus raphanistrum, exhibits tetradynamous stamens (four long and two short, producing a dimorphism in anther height within each flower), as do the vast majority of the more than 3000 species in the Brassicaceae. Here we examine the hypothesis that selection maintains the stasis of dimorphic anther height by investigating the effects of this trait on pollen removal, seed siring success, and seed set in R. raphanistrum using both experimental and observational methods. Observational selection gradient analysis based on lifetime seed siring success provided evidence for an optimum dimorphism that was greater than zero in one of three years. In both experimentally manipulated and unmanipulated flowers, more pollen was removed in single visits from flowers with less dimorphism. There was no significant effect of anther dimorphism on female fitness (seed set). Therefore, there is some evidence to suggest that selection is maintaining anther dimorphism in wild radish, and that higher male fitness might result from restriction of single-visit pollen removal. We discuss these results in light of pollen presentation theory.
Literature Cited
- Barnes, M. G. 2001. Development and evolution of the tetradynamous stamen condition in the Brassicaceae. B.A. thesis, Reed College, Portland , OR .
-
Barrett, S. C. H.
1992. Evolution and function of heterostyly. Springer-Verlag,
Berlin
.
10.1007/978-3-642-86656-2 Google Scholar
- Campbell, D. R., N. M. Waser, M. V. Price, E. A. Lynch, and R. J. Mitchell 1991. Components of phenotypic selection: Pollen export and flower corolla width in Ipomopsis aggregata. Evolution. 45: 1458–1467.
- Caruso, C. M. 2000. Competition for pollination influences selection on floral traits of Ipomopsis aggregata. Evolution. 54: 1546–1557.
- Conner, J. K., and S. Rush 1996. Effects of flower size and number on pollinator visitation to wild radish, Raphanus raphanistrum. Oecologia. 105: 509–516.
- Conner, J. K., and S. Via 1993. Patterns of phenotypic and genetic correlations among morphological and life-history traits in wild radish, Raphanus raphanistrum. Evolution. 47: 704–711.
- Conner, J. K., R. Davis, and S. Rush 1995. The effect of wild radish floral morphology on pollination efficiency by four taxa of pollinators. Oecologia. 104: 234–245.
- Conner, J. K., S. Rush, and P. Jennetten 1996a. Measurements of natural selection on floral traits in wild radish (Raphanus raphanistrum). I. Selection through lifetime female fitness. Evolution. 50: 1127–1136.
- Conner, J. K., S. Rush, S. Kercher, and P. Jennetten 1996b. Measurements of natural selection on floral traits in wild radish (Raphanus raphanistrum). II. Selection through lifetime male and total fitness. Evolution. 50: 1137–1146.
- Cresswell, J. E. 1998. Stabilizing selection and the structural variability of flowers within species. Ann. Bot.. 81: 463–473.
- 2000. Manipulation of female architecture in flowers reveals a narrow optimum for pollen deposition. Ecology. 81: 3244–3249.
- Escaravage, N., E. Flubacker, A. Pornon, B. Doche, and I. Till-Bottraud 2001. Stamen dimorphism in Rhododendron ferrugineum (Ericaceae): development and function. Am. J. Bot. 88: 68–75.
- Galen, C. 1989. Measuring pollinator-mediated selection on morphometric traits: bumblebees and the alpine sky pilot, Polemonium viscosum. Evolution. 43: 882–890.
- Galen, C., and M. L. Stanton 1989. Bumble bee pollination and floral morphology: Factors influencing pollen dispersal in the alpine sky pilot, Polemonium viscosum (Polemoniaceae). Am. J. Bot.. 76: 419–426.
- Galloway, G. L., R. L. Malmberg, and R. A. Price 1998. Phylogenetic utility of the nuclear gene arginine decarboxylase: an example from Brassicaceae. Mol. Biol. Evol.. 15: 1312–1320.
-
Gould, S. J.
2002. The structure of evolutionary theory. Harvard Univ. Press,
Cambridge
,
MA
.
10.2307/j.ctvjsf433 Google Scholar
- Harder, L. D. 1990. Pollen removal by bumble bees and its implications for pollen dispersal. Ecology. 71: 1110–1125.
- Harder, L. D., and S. C. H. Barrett 1993. Pollen removal from tristylous Pontederia cordata: effects of anther position and pollinator specialization. Ecology. 74: 1059–1072.
- Harder, L. D., and J. D. Thomson 1989. Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. Am. Nat.. 133: 323–344.
- Karoly, K., and J. K. Conner 2000. Heritable variation in a family-diagnostic trait. Evolution. 54: 1433–1438.
- Kingsolver, J. G., H. E. Hoekstra, J. M. Hoekstra, D. Berrigan, S. N. Vignieri, C. E. Hill, A. Hoang, P. Gibert, and P. Beerli 2001. The strength of phenotypic selection in natural populations. Am. Nat.. 157: 245–261.
- Kobayashi, S., K. Inoue, and M. Kato 1999. Mechanism of selection favoring a wide tubular corolla in Campanula punctata. Evolution. 53: 752–757.
- Lande, R., and S. J. Arnold 1983. The measurement of selection on correlated characters. Evolution. 37: 1210–1226.
- Maynard Smith, J., R. Burian, S. Kauffman, P. Alberch, J. Campell, B. Goodwin, R. Lande, D. Raup, and L. Wolpert 1985. Developmental constraints and evolution. Q. Rev. Biol.. 60: 265–287.
- Morgan, M. T., and J. K. Conner 2001. Using genetic markers to directly estimate male selection gradients. Evolution. 55: 272–281.
- Murcia, C. 1990. Effect of floral morphology and temperature on pollen receipt and removal in Ipomoea trichocarpa. Ecology. 71: 1098–1109.
- Preston, R. E. 1986. Pollen-ovule ratios in the Cruciferae. Am. J. Bot.. 73: 1732–1740.
- Price, R. A., J. D. Palmer, and I. A. Al-Shehbaz 1994. Systematic relationships of Arabidopsis: a molecular and morphological perspective. Pp. 7–19 in E. M. Meyerowitz and C. R. Somerville, eds Arabidopsis. Cold Spring Harbor Laboratory Press, Plain-view , NY .
- Rush, S., J. K. Conner, and P. Jennetten 1995. The effects of natural variation in pollinator visitation on rates of pollen removal in wild radish, Raphanus raphanistrum (Brassicaceae). Am. J. Bot.. 82: 1522–1526.
- SAS Institute. 1994. JMP. SAS Institute Inc., Cary , NC .
- Schemske, D. W., and C. C. Horvitz 1989. Temporal variation in selection on a floral character. Evolution. 43: 461–465.
- Schluter, D. 1988. Estimating the form of natural selection on a quantitative trait. Evolution. 42: 849–861.
- Stanton, M. L. 1994. Male-male competition during pollination in plant populations. Am. Nat.. 144: S40–S68.
- Stanton, M. L., H. J. Young, N. C. Ellstrand, and J. M. Clegg 1991. Consequences of floral variation for male and female reproduction in experimental populations of wild radish, Raphanus sativus L. Evolution. 45: 268–280.
- Stanton, M. L., A. A. Snow, S. N. Handel, and J. Bereczky 1989. The impact of a flower-color polymorphism on mating patterns in experimental populations of wild radish (Raphanus raphanistrum L.). Evolution. 43: 335–346.
- Stanton, M. L., T.-L. Ashman, and L. F. Galloway 1992. Estimating male fitness of plants in natural populations. Pp. 62–90 in R. Wyatt, ed Ecology and evolution of plant reproduction. Chapman and Hall, NY .
- Stearns, S. C. 1994. The evolutionary links between fixed and variable traits. Acta Palaeontol. Pol.. 38: 215–232.
- Stone, J. L., and J. D. Thomson 1994. The evolution of distyly: Pollen transfer in artificial flowers. Evolution. 48: 1595–1606.
- Thomson, J. D., and B. A. Thomson 1992. Pollen presentation and viability schedules in animal-pollinated plants: Consequences for reproductive success. Pp. 1–24 in R. Wyatt, ed Ecology and evolution of plant reproduction. Chapman and Hall, NY .
-
Waser, N. M.
1983. The adaptive nature of floral traits: Ideas and evidence. Pp. 241–285
in
L. Real, ed
Pollination biology. Academic Press,
Orlando
,
FL
.
10.1016/B978-0-12-583980-8.50017-X Google Scholar
- Wolfe, L. M., and S. C. H. Barrett 1989. Patterns of pollen removal and deposition in tristylous Pontederia cordata L. (Pontederiaceae). Biol. J. Linn. Soc.. 36: 317–329.
- Zomlefer, W. R. 1994. Guide to flowering plant families. Univ. of North Carolina Press, Chapel Hill , NC .